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Review Article Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Academy of Cardiovascular and Pulmonary Rehabilitation Yuan-Yang Cheng a,b, Chin-Ming Chen c,d,e, Wei-Chun Huang b,f,g,h, Shang-Lin Chiang i,j, Pei-Chun Hsieh k,l, Ko-Long Lin m, Yi-Jen Chen n,o,p,q, Tieh-Cheng Fu r,s,t, Shu-Chun Huang t,u,v,w, Ssu-Yuan Chen x,y, Chia-Hsin Chen n,o,q, Shyh-Ming Chen t,z, Hsin-Shui Chen aa,ab, Li-Wei Chou ac,ad,ae, Chen-Liang Chou b,af, Min-Hui Li m, Sen-Wei Tsai ag,ah, Lin-Yi Wang t,ai, Yu-Lin Wang aj,ak, Willy Chou aj,ak,* a Department of Physical Medicine and Rehabilitation, Veterans General Hospital, No.1650 Taiwan Boulevard Sect. 4, Taichung, Taiwan b School of Medicine, National Yang-Ming University, No. 155, Sec. 2, Linong Street, , Taiwan c Department of Intensive Care Medicine, Chi-Mei Medical Center, No. 901, Zhonghua Rd., Yongkang Dist., , Taiwan d Center for Quality Management, Chi-Mei Medical Center, No. 901, Zhonghua Rd., Yongkang Dist., Tainan, Taiwan e School of Medicine, Chung Shan Medical University, Taichung, Taiwan f Department of Critical Care Medicine and Cardiology Center, Veterans General Hospital, No. 386, Dazhong 1st Rd., Zuoying Dist., Kaohsiung, Taiwan g Department of Physical Therapy, Fooyin University, No. 151 Jinxue Rd., Daliao Dist., Kaohsiung, Taiwan h Graduate Institute of Clinical Medicine, Kaohsiung Medical University, No. 100, Shin-Chuan 1st Rd., Sanmin Dist., Kaohsiung, Taiwan i Department of Physical Medicine and Rehabilitation, Tri-Service General Hospital, No.325, Sec.2, Chenggong Rd., Neihu , Taipei, Taiwan j School of Medicine, National Defense Medical Center, No. 161, Sec. 6, Minquan E. Rd., Neihu Dist., Taipei, Taiwan k Department of Physical Medicine and Rehabilitation, National Cheng Kung University Hospital, No. 138, Sheng Li Rd., Tainan, Taiwan

* Corresponding author. No. 901, Chung Hwa Rd., Yongkang District, Tainan City, 710, Taiwan. Fax: +886 6 7266787. E-mail address: [email protected] (W. Chou). https://doi.org/10.1016/j.jfma.2020.08.015 0929-6646/Copyright ª 2020, Formosan Medical Association. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL 2 l Institute of Clinical Medicine, National Cheng Kung University, No. 1, University Rd., Tainan, Taiwan m Department of Physical Medicine and Rehabilitation, Kaohsiung Veterans General Hospital, No. 386, Dazhong 1st Rd., Zuoying Dist., Kaohsiung, Taiwan n Department of Physical Medicine and Rehabilitation, Kaohsiung Medical University Hospital, No. 100, Tzyou 1st Rd., Sanmin Dist., Kaohsiung, Taiwan o Department of Physical Medicine and Rehabilitation, School of Medicine, Kaohsiung Medical University, No. 100, Shin-Chuan 1st Rd., Sanmin Dist., Kaohsiung, Taiwan p Department of Physical Medicine and Rehabilitation, Kaohsiung Municipal Siaogang Hospital, No. 482, Shanming Rd, Siaogang Dist., Kaohsiung, Taiwan q Regenerative Medicine and Cell Therapy Research Center, Kaohsiung Medical University, No. 100, Tzyou 1st Rd., Sanmin Dist., Kaohsiung, Taiwan r Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, , No. 222, Maijin Rd., Anle Dist., Keelung, Taiwan s Heart Failure Research Center, Division of Cardiology, Department of Internal Medicine, Chang Gung Memorial Hospital, Keelung, No. 222, Maijin Rd., Anle Dist., Keelung, Taiwan t School of Medicine, College of Medicine, Chang Gung University, No. 259, Wenhua 1st Rd., Guishan Dist., Taoyuan, Taiwan u Department of Physical Medicine and Rehabilitation, New Taipei Municipal TuCheng Hospital, Chang Gung Memorial Hospital, No. 6, Sec. 2, Jincheng Rd., Tucheng Dist., , 236, Taiwan v Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Linkou, No. 5, Fuxing St., Guishan Dist., Taoyuan, Taiwan w Healthy Aging Research Center, Chang Gung University, No. 259, Wenhua 1st Rd., Guishan Dist., Taoyuan, Taiwan x Division of Physical Medicine and Rehabilitation, Fu Jen Catholic University Hospital, School of Medicine, College of Medicine, Fu Jen Catholic University, No. 69, Guizi Rd., Taishan District, New Taipei City, Taiwan y Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital and National Taiwan University College of Medicine, No. 1, Changde St., Zhongzheng Dist., Taipei, Taiwan z Section of Cardiology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, No. 123, Dapi Rd., Niaosong Dist., Kaohsiung, Taiwan aa Department of Physical Medicine & Rehabilitation, National Taiwan University Hospital, Yunlin Branch, No.579, Sec. 2, Yunlin Rd., Douliu City, Yunlin, Taiwan ab PHD Program of College of Medicine, China Medical University, No. 2, Yuh-Der Rd., Taichung, Taiwan ac Department of Physical Medicine and Rehabilitation, China Medical University Hospital, No. 91, Hsueh-Shih Rd., Taichung, Taiwan ad Department of Physical Therapy and Graduate Institute of Rehabilitation Science, China Medical University, No. 91, Hsueh-Shih Rd., Taichung, Taiwan ae Department of Rehabilitation, Asia University Hospital, No. 500, Lioufeng Rd., Wufeng, Taichung, Taiwan af Department of Physical Medicine & Rehabilitation, Taipei Veterans General Hospital, No. 201, Sec. 2, Shipai Rd., , Taipei, Taiwan ag Department of Physical Medicine and Rehabilitation, Taichung Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, No. 88, Sec. 1, Fengxing Rd., Tanzi Dist., Taichung, Taiwan ah School of Medicine, Tzu Chi University, No. 701, Zhongyang Rd., Sec. 3, Hualien, Taiwan ai Department of Physical Medicine and Rehabilitation, Kaohsiung Chang Gung Memorial Hospital, No. 123, Dapi Rd., Niaosong Dist., Kaohsiung, Taiwan aj Department of Physical Medicine and Rehabilitation, Chi Mei Medical Center, No. 901, Zhonghua Rd., Yongkang Dist., Tainan, Taiwan ak Center of General Education, Southern Taiwan University of Science and Technology, No. 1, Nan-Tai Street, Yongkang Dist., Tainan, Taiwan

Received 21 May 2020; received in revised form 9 August 2020; accepted 10 August 2020

KEYWORDS The COronaVIrus Disease 2019 (COVID-19), which developed into a pandemic in 2020, has Consensus; become a major healthcare challenge for governments and healthcare workers worldwide. COVID-19; Despite several medical treatment protocols having been established, a comprehensive reha- Infection control; bilitation program that can promote functional recovery is still frequently ignored. An online

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL Rehabilitation for COronaVIrus Disease 2019 3

consensus meeting of an expert panel comprising members of the Taiwan Academy of Cardio- Rehabilitation vascular and Pulmonary Rehabilitation was held to provide recommendations for rehabilitation protocols in each of the five COVID-19 stages, namely (1) outpatients with mild disease and no risk factors, (2) outpatients with mild disease and epidemiological risk factors, (3) hospitalized patients with moderate to severe disease, (4) ventilator-supported patients with clear cogni- tive function, and (5) ventilator-supported patients with impaired cognitive function. Apart from medications and life support care, a proper rehabilitation protocol that facilitates recov- ery from COVID-19 needs to be established and emphasized in clinical practice. Copyright ª 2020, Formosan Medical Association. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/).

The role of rehabilitation and infection and gloves, are still needed. Moreover, health care precautions in the management of personnel require extra training regarding infection pre- COronaVIrus Disease 2019 infection cautions, such as in the event of accidental endotracheal tube disconnection from the ventilator. Only under proper protection against COVID-19 transmission can rehabilita- Since the end of 2019, COronaVIrus Disease 2019 (COVID- tion programs be safely implemented and function as 19), a novel infectious disease emerging from Wuhan, intended for the management of affected patients. How- China, has continued to spread rapidly, causing an ongoing ever, the recommendations provided in this expert global outbreak. Patients may exhibit dyspnea, hypoxia, consensus should neither replace local institutional pol- remarkable pneumonia, acute respiratory distress syn- 1,2 icies nor substitute clinical decisions established by phy- drome (ARDS), or even multiple organ failure. In addition sicians for any patient. to the possible sequelae of pulmonary fibrosis,3 which could impair the survivors’ ventilation and oxygenation, many other organs could be affected, especially the cardiovas- cular system.4 Common complications of the cardiovascular Risk factors and categorization for patients system may include arrhythmia, myocarditis, acute coro- with COVID-19 nary syndrome, venous thromboembolism, cardiogenic shock, and heart failure.5 Furthermore, prolonged inac- Considering that COVID-19 can cause significant morbidity tivity can also affect exercise capacity significantly. Apart and mortality based on certain risk factors, such risk factors from medical treatment and supportive therapy, rehabili- need to be identified in order to establish individualized tation plays a vital role throughout the entire disease rehabilitation programs. Data from 44,672 laboratory- course. An appropriate rehabilitation program could help confirmed cases of COVID-19 in China have shown that patients with mild disease maintain exercise capacity and disease severity can be categorized as mild, severe, and activities of daily living. For patients with advanced disease critical.1 Approximately 81% of infected patients were severity, a well-designed rehabilitation program is even categorized as mild and presented without or with mild more crucial to improve pulmonary secretion clearance, pneumonia, while approximately 14% were categorized as ameliorates side-effects related to a prolonged bedridden severe and presented with dyspnea, blood oxygen satura- state, and even prevents intensive care unit-acquired tion 93%, partial pressure of arterial oxygen to fraction of weakness. This expert consensus provides recommenda- inspired oxygen (P/F) ratio <300, or lung infiltrates >50% tions for rehabilitating patients with varying degrees of within 24e48 h. The remaining 5% were classified as critical COVID-19 severity. and presented with respiratory failure, septic shock, or Although rehabilitation has multiple benefits for pa- multiple organ dysfunction, which resulted in a high mor- tients, the disease remains highly contagious and poses a tality rate of 49%. Those with preexisting comorbid condi- substantial threat to medical providers. Hence, proper tions, including cardiovascular disease (CVD) (10.5%), protective personal equipment (PPE) should be used when diabetes (7.3%), chronic respiratory disease (6.3%), hyper- caring for patients with COVID-19,6 while patients should tension (6.0%), and cancer (5.6%), displayed a higher case- always be wearing surgical masks during rehabilitation. fatality rate (CFR). Patients without underlying medical Health care workers should be under airborne precautions conditions had an overall CFR of 0.9%. A recent meta- wearing PPE, including N95 masks, fluid resistant long- analysis that assessed the risk for severe infection in sleeved gowns, face shields, and gloves, when perform- 46,248 patients7 found that those with CVD [odds ratio ing chest physiotherapy on non-intubated patients or (OR) Z 3.42] had the highest risk for severe infection, aerosol-generating procedures during ventilator discon- followed by respiratory system disease (OR Z 2.46) and nection of intubated patients. Even during early mobili- hypertension (OR Z 2.36). Moreover, another study outside zation of intubated patients with a closed ventilator China showed that older age (OR Z 1.06), male gender circuit, droplet precautions wearing PPE, including surgi- (OR Z 3.68), and hypertension (OR Z 2.71) were inde- cal masks, fluid-resistant long-sleeved gowns, face shields pendently associated with severe disease at admission.8

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL 4 Y.-Y. Cheng et al.

Altogether, potentially significant risk factors for severe On the other hand, resistance training involves single- or COVID-19 that should be identified and considered when multi-joint exercises targeting major muscles including the designing rehabilitation programs include old age, male biceps, triceps brachii, pectoralis major, rhomboideus, gender, hypertension, diabetes, respiratory disease, and gluteus, iliopsoas, quadriceps, hamstring, anterior tibialis, CVD. and calf muscles, using weight machines, free weights, or The World Health Organization (WHO) had categorized body weight. Training frequency, intensity and duration clinical syndromes associated with COVID-19 as mild illness, should be as follows: pneumonia, severe pneumonia, ARDS, sepsis and septic shock.9 However, this expert consensus categorized pa- - Frequency: 2e3 days per week with at least 48-h tients with COVID-19 differently such that outpatients with intervals various risk factors or inpatients with disparate cognitive - Intensity: strength training involves using a weight status should receive distinct rehabilitation programs. equivalent of 60%e70% of the one repetition maximum, Therefore, the current expert consensus categorized pa- while endurance training involves using a weight equiv- tients with COVID-19 into the following five groups: (1) alent to less than 50% of the one repetition maximum. outpatients with mild disease and no risk factors, (2) out- The one repetition maximum refers to the maximum patients with mild disease and epidemiological risk factors, amount of weight that a person can possibly lift for only (3) hospitalized patients with moderate to severe disease, one time.15 (4) ventilator-supported patients with clear cognitive - Duration: 2e4 sets with 8e12 repetitions for strength function, and (5) ventilator-supported patients with training; 2 sets with 15e25 repetitions for endurance impaired cognitive function. training.

After exercise training, a 5e10 min cool-down consisting Suggestions for the rehabilitation of of light intensity endurance activities, followed by at least 10 min of stretching exercises, should be performed. outpatients with mild disease and no risk The current COVID-19 management guideline recom- factors mends cancelling elective procedures16 and prefers home- based self-monitored rehabilitation, with adequate envi- Majority of the patients with COVID-19 had mild disease.1 ronmental disinfection. Moreover, emerging studies have Those with mild disease and no risk factors were allo- found that tele-rehabilitation and self-rehabilitation tuto- cated to home care, with rehabilitation recommendations rials may be helpful.17 Certain traditional Chinese health- similar to those of the American College of Sports Medi- promoting exercises (Baduanjin qigong, Tai Chi, etc.) cine (ACSM) general principles of exercise prescription,10 have been recommended by Chinese rehabilitation studies though infection control is essential.11,12 While home- for patients with COVID-1918 and could complement formal based rehabilitation is recommended for this group of exercise training. However, patients developing unstable patients, hospital-based rehabilitation may be started vital signs or respiratory distress must discontinue only when patients have been (1) at least 10 days since exercise.10,18 symptom onset (2) at least 24 h since resolution of fever Current understanding on COVID-19 suggests that preg- without taking antipyretic drugs and (3) without other nant women present with similar clinical findings as non- COVID-19 related symptoms, according to the recom- pregnant adults.19 Therefore, pregnant women can also mendation for discontinuation of home isolation from maintain their exercise programs as recommended by the Center for Disease Control and Prevention of United ACSM. However, exercise in the supine position should be States.13 The objective of rehabilitation is primarily avoided after week 16 of pregnancy given its tendency to preventing complications of inactivity through condi- reduce venous return due to the weight of fetus. Further- tioning exercises. more, pregnant women should also avoid contact sports, Conditioning exercises should include at least three exercising in hot humid environments, or Valsalva maneu- components, namely warm-up, exercise, cool-down and ver during exercise. On the other hand, children with stretching.10 A proper warm-up generally includes light COVID-19 usually have less severe symptoms than adults20 intensity endurance activities for at least 5e10 min. Ex- and constitute a special group that needs extra physical ercises include both aerobic exercise and resistance activity to prevent a sedentary lifestyle. Unlike adults, training. Aerobic training involves the activation of large children need at least 60 min of aerobic training daily. muscle groups in a rhythmic movement (e.g., treadmill However, due to their immature thermoregulatory mecha- walking, bicycling, or upper limb ergometer trainings). nism, children also need to avoid exercising in hot humid Training frequency, intensity, and duration should be as environments. follows: Suggestions for the rehabilitation of - Frequency: 5 days or more per week - Intensity: maintaining a heart rate reserve of 40%e59% outpatients with mild disease and during exercise, while the heart rate reserve refers to epidemiological risk factors the difference between the predicted maximum heart rate and the resting heart rate14 Although most patients with COVID-19 develop mild dis- - Duration: 30e60 min ease,1 those with preexisting comorbid conditions, such as

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL Rehabilitation for COronaVIrus Disease 2019 5

CVD, diabetes, chronic respiratory disease, and hyperten- efficient breathing.24 Inspiratory muscle training, sion, are at greater risk for developing critical illness and with a threshold loading starting at 30% of the higher CFR compared to those without such conditions.7 In maximal inspiratory pressure (MIP), is recommended this group of patients, home-based outpatient programs given evidence suggesting its benefits in reducing with proper video instructions and tele-rehabilitation are dyspnea and improving, exercise capacity and quality still recommended to avoid COVID-19 transmission. A of life for patients with COPD.25 During conditioning comprehensive exercise program including aerobic and exercises, intensity should be set at a rated perceived resistance training, as previously mentioned, could be exertion of 4e6ona0e10 scale. Exercise in cold provided to patients with comorbidities under the following environments or those with allergens or pollutants special consideration: should be limited to avoid triggering bronchocon- striction among susceptible individuals. (1) Hypertension: Post-exercise blood pressure (BP) (4) Diabetes mellitus (DM): Blood glucose levels should be reduction should be considered especially among assessed before and after exercise. Symptoms asso- older patients receiving anti-hypertensive medicine ciated with hypoglycemia, including tingling of the such as a-blockers and vasodilators. Therefore, ex- mouth and fingers, tremor, abnormal sweating, anx- ercise termination should be gradual, while the cool- iety, confusion, amnesia, hunger, and visual distur- down phase should be extended and monitored bances, should be carefully monitored. Individuals carefully until BP and heart rate return to resting with retinopathy should avoid vigorous activities and levels. Avoid the Valsalva maneuver or breath holding Valsalva maneuver, which may dramatically elevate during resistance training and static stretching to BP. Those with polyneuropathy require proper foot avoid excessive BP elevation. care to prevent foot ulcers and the risk of (2) CVD: Exercise training is safe and effective for most amputation. patients with CVD. Patient whose angina threshold heart rate had been previously determined by a Despite home-based rehabilitation is suggested for this formal cardiopulmonary exercise test should adjust group of patients, several contraindications for exercise, as their exercise intensity to the upper limit of heart shown in Table 1,10 should be reminded for both healthcare rate 10 beats/min below the angina threshold.21 Pa- providers and patients. In the event of any adverse events tients who had not undergone formal exercise testing encountered by patients during home-based rehabilitation, can exercise at a rated perceived exertion of 4e6on exercise training should be stopped immediately. For pa- a0e10 scale.21 However, a formal exercise test tients with angina symptoms or significant hypertension, should still be considered in patients with advanced sublingual nitroglycerin or short acting calcium channel CVD with proper clinical disinfection following CDC11 blocker could be taken respectively. For patients with hy- and WHO12 recommendations. Routine assessment potensive responses, prompt lying done with fluid supply of exercise intolerance symptoms, such as dyspnea, should be implemented. For patients experiencing hypo- lightheadedness or dizziness, palpitations, chest glycemic symptoms, sugar cubes should be given promptly. tightness, and pain, should be carefully performed. For patients with acute exacerbating symptoms of asthma For patients with very limited exercise capacities, or COPD, short-acting bronchodilator inhalation should be multiple shorter (i.e., <10 min) exercise sessions may used first. If the patients’ vital signs and symptoms still not be considered initially. Patients with heart failure recover, emergent medical support should be called for should begin aerobic training several weeks before help without hesitation. resistance training.10 Some medications used for treatment of COVID-19 may induce heart rhythm problems including QT interval prolongation and Suggestions for rehabilitation of hospitalized conduction block. These medications include patients with moderate to severe disease hydroxychloroquine, antiviral drugs such as favipir- avir and lopinavir/ritonavir, and antibiotics such as Approximately 14% of patients with COVID-19 developed 22 azithromycin. Despite hydroxychloroquine no moderate to severe disease that required hospitalization 23 longer recommended in treating COVID-19, when and aggressive treatment.1 These individuals usually pre- patients taking these medications experience unusual sent with fever, cough, dyspnea, tachycardia, tachypnea, symptoms of palpitation, formal electrocardiogram and various degrees of oxygen desaturation necessitating should be arranged after cardiologist consultation support.2 Studies have shown that early rehabilitation in- before further exercise training. terventions for community-acquired pneumonia and inter- (3) Pulmonary disease: Patients with previous chronic stitial pneumonia within 2 days of admission reduced in- pulmonary diseases could develop much more airway hospital mortality.26,27 The two primary objectives of secretions than those without. Airway clearance rehabilitation in this stage are promoting airway clearance techniques, which will be described in detail in the and preventing complications of acute illness-related next section, should include flutter breathing, auto- immobilization. genic drainage, and cough techniques, such as huff About 33.7% of COVID-19 patients could have copious coughing and controlled coughing. Specific exercises, sputum production.28 Incorporating chest physiotherapy such as Yoga, Tai-chi, Pilates, and trunk core muscle into the medical treatment of patients with lung consoli- training, can help stabilize the trunk and promote dation plays an important role in helping patients with

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL 6 Y.-Y. Cheng et al.

(5) Flutter breathing: This technique utilizes a device Table 1 Contraindications for home exercise training for containing a movable steel ball in a sealed pipe. The patients with COVID-19. patient rapidly blows air into the pipe, which shakes COVID-19 Contraindications the steel ball and produces rhythmic airflow. Flutter patients group breathing could ultimately loosen the sputum within 31 Without Acute high fever > 39 C the airway. underlying Tachypnea at rest > 30 breaths per diseases minutes Another important issue in the rehabilitation of patients With Uncontrolled resting with moderate to severe disease is preventing decondi- hypertension hypertension > 180/110 mmHg tioning due to acute illness. Immobilization has been shown Orthostatic blood pressure drop to speed functional decline with reduced muscle strength of > 20 mmHg with symptoms and cardiorespiratory fitness, particularly among elderly 1,35 With DM Blood sugar < 70 mg/dl individuals and those with comorbidities. Therefore, Blood sugar > 300 mg/dl with urine once medical condition stabilized, early mobilization 36 ketones should be encouraged. Rehabilitation interventions for With CVD Unstable angina such patients should include the following: Uncontrolled sinus tachycardia > 120 beats per minute (1) Active or active-assisted range of motion (ROM) ex- History of significant aortic stenosis ercise: Patients with moderate to severe disease who (aortic valve area < 1.0 cm2) are able to actively move their extremities are History of third-degree atrioventricular encouraged to engage in active or active-assisted block without pacemaker ROM exercises to maintain or improve joint integrity Uncontrolled atrial or ventricular and prevent joint contracture and soft-tissue 37 arrhythmias shortening. Uncompensated heart failure (2) Mobilization and progressive off-bed activities: early With pulmonary Acute exacerbated symptoms of mobilization with progressive mobility training, diseases preexisting COPD or asthma including off-bed transferring, unsupported sitting, standing, level-surface ambulation, and stair climb- Abbreviations: CVD, cardiovascular disease; COPD, chronic obstructive pulmonary disease; COVID-19, COronaVIrus Disease ing, tailored to the patient’s general condition should 2019; DM, diabetes mellitus. be carried out once medically stabilized. Proper walking aid may be used to assist in energy conser- vation to reduce distress during the activity. (3) Aerobic exercise: aerobic exercise using a stationary airway secretions. Proper chest physiotherapy could pro- bike, arm ergometer, or level-surface walking begin- mote effective expectoration, enhance mucociliary clear- ning with light intensity (<3.0 metabolic equivalents) ance of secretions to the upper airways, and improve cough should be performed. Aerobic exercise intensity can 29 effectiveness. Chest physiotherapy strategies that pro- also be assessed and modified according to the pa- mote airway clearance include the following: tient’s rating of perceived exertion. The duration of aerobic exercise can be cumulative, starting at (1) Positioning: Optimal positioning to reduce dyspnea 5e10 min per training session, based on the patient’s should be patient specific. For instance, an upright, exercise tolerance. forward-leaning position with arm support will reduce dyspnea and respiratory distress, particularly among When performing rehabilitation interventions, close patients with COPD. A side-lying position may opti- monitoring of vital sign changes is imperative given that the mize perfusion to the good lung during unilateral lung patients’ condition may progress. For patients with COVID- disease, thus improving gas exchange.30 19 confined to isolation rooms, alternative approaches, (2) Active cycle of breathing techniques (ACBT): ACBT such as supervised telerehabilitation, should be incorpo- requires patient’s active participation in guided rated to avoid direct contact between health care workers breathing control to mobilize airway secretions and and the patients. reduce dyspnea.31 (3) Chest percussion and vibration: chest wall oscillation, mechanical vibration and chest percussion facilitate Suggestions for the rehabilitation of ventilator- sputum expectoration particularly among patients supported patients with clear cognitive status with copious airway secretions.32,33 (4) Huffing and controlled coughing: Huffing is charac- The rehabilitation of ventilator-supported patients with terized by rapid air exhalation without glottis severe COVID-19 is similar to that of patients with respi- closure, while controlled coughing aims to avoid ratory failure caused by other viral pneumonia infections. shallow and inefficient coughs. Both coughing tech- Intubated patients with a closed ventilator circuit have a niques have been shown to reduce coughing effort lower risk for droplet transmission compared to non- 34 and improve airway clearance. intubated patients. However, certain aerosol-generating

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL Rehabilitation for COronaVIrus Disease 2019 7 procedures during ventilator circuit disconnection, such percussive ventilation, HFCWO has been shown to as oropharyngeal suctioning, cough technique training, reduce dyspnea and improve pulmonary function.46 and inspiratory muscle training, require proper use of PPE Apart from clearing airway secretions, prone posi- under airborne precautions to reduce the risk of virus tioning, which is best performed early in the disease transmission. Airborne infection isolation rooms and course (ideally within 48 h) when the P/F ratio is careful procedure execution should be utilized to mini- <150 mmHg, continues to play a vital role in the mize the risk of virus exposure during patient contact. management of ARDS.47 Combined with low tidal Telerehabilitation, computer-assisted rehabilitation, and volume ventilation (around 6 mL/kg), recommenda- virtual reality technology might be useful for ventilated tions suggest that prone positioning be maintained for patients in intensive care units.38,39 However, rehabilita- 16 h daily.47 Prone positioning has been shown to tion should be abandoned when patients exhibit promote significant improvements in gas exchange decreased oxygen saturation despite inhaled oxygen >50% and oxygenation. A side-lying position with the and positive end expiratory pressure (PEEP) >10 cm H2O, diseased lung on the top may also help improve newly onset arrhythmia or coronary ischemia, systolic BP ventilation and perfusion. >200 mmHg or mean BP <60 mmHg despite medication, and uncontrolled high fever or seizures.40 The following are the key points and strategies for the rehabilitation of ventilated patients with clear cognitive Suggestions for the rehabilitation of ventilator- status: supported patients with impaired cognitive status (1) Activities: In-bed cycling in patients with critical illness has been shown to be a safe and feasible As mentioned previously, 5% of patients with COVID-19 procedure for preserving muscle function41 and became critically ill and required admission to intensive muscle fiber cross-sectional area,42 as well as care units and mechanical ventilation.1 Despite early fostering positive mental effect, including the feeling rehabilitation within the first 72 h following intubation may of control, safety, and hope, during the critical stages benefit patients with acute respiratory failure by prevent- of the illness.43 Low resistance levels (i.e., approxi- ing intensive care unit-acquired complications,48 limited mately 0.5 Nm), are recommended with patient self- options are available for patients with impaired cognitive selected pedaling rate for 30 min daily.41 Upper-limb status. The following are the recommended strategies for resistance training using elastic bands and pulleys can this group of patients: also be utilized. Patients who have stable clinical status can commence out-of-bed mobility depending (1) For patients with severe ARDS and impaired cogni- on their tolerance, which may include sitting on the tion, prone ventilation is still suggested for 16 h edge of the bed, moving from bed to chair, standing daily, which is to be repeated until a P/F ratio of next to the bed, stepping on the spot, and walking 150 mmHg with a PEEP of 10 cm H2Oanda 44 with ambulatory assistive devices. fraction of inspired oxygen (FiO2) 0.60 are ach- (2) Breathing exercises: Inspiratory muscle training, ieved for at least 4 h after supine positioning.49 On which strengthens the inspiratory muscles through the other hand, prone ventilation may increase the the application of resistance during inspiration, can risk of pressure sores and endotracheal tube also be used for intubated patients or those with a obstruction.50 tracheostomy. Using a threshold training device, with (2) In cases of hypersecretion and ineffective mucus the threshold set at 50% of the MIP, five sets of six clearance, airway clearance techniques, such as 45 breaths performed once per day are recommended. chest percussion, vibration, and postural drainage Patients can also be educated on diaphragmatic every 4e6 h have been widely employed for me- breathing, which involves the negative pressure chanically ventilated patients.51 Intrapulmonary generated by the diaphragm instead of the accessory percussive ventilation52 and HFCWO can also be respiratory muscles. Finally, chest expansion and implemented to help sputum loosening. Sputum mobilization are important for increasing chest wall suction should be done under airborne precautions. mobility and improving thoracic compliance during (3) Diaphragmatic facilitation technique involves exert- mechanical ventilation. ing a downward and cephalad pressure to the dia- (3) Chest care and airway secretions management: phragm during exhalation for the purpose of Postural drainage, percussion, vibration, and airway stretching to facilitate subsequent diaphragmatic suctioning can be used to minimize pulmonary contraction during ventilator air pumping.53 This secretion retention and maximize oxygenation. High- technique can be used for patients with both clear frequency chest wall oscillation (HFCWO), which and impaired cognitive function. utilizes a percussive vest that replaces manual (4) Frequent postural change in bed is important for pre- involvement, can better facilitate mucus movement venting bedsores. Passive ROM exercise involving the towards the central airway. The device usually major joints of the four limbs is vital for maintaining operates between 7 and 15 Hz on intubated patients. soft-tissue length and preventing joint contracture. Although less effective than intrapulmonary Each upper and lower extremity joint should perform

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL 8 Y.-Y. Cheng et al.

Figure 1 The flowchart of suggested rehabilitation interventions and infection precautions for patients with COVID-19. The rehabilitation protocols for each of the five categories of patients with COVID-19 are summarized in this flowchart, and the infection precautions during contacting these patients are included as well. Abbreviations: COPD, chronic obstructive pulmonary disease; COVID-19, Coronavirus Disease 2019; CVD, cardiovascular disease; DM, diabetes mellitus; HFCWO, high frequency chest wall oscillation; PPE, personal protective equipment.

5e10 repetitions in the supine position once or twice Funding/Support statement per day.54,55 Chest wall mobilization and expansion should also be performed in this group of patients to None declared. maintain thoracic compliance.

Conclusions Declaration of Competing Interest

Patients with COVID-19 often suffer from reduced car- The authors have no conflicts of interest relevant to this diopulmonary endurance and impaired quality of life after article. recovery because of the possible sequelae of pulmonary fibrosis,3 as well as the inevitable consequences of long- term bedridden status during treatment. On the other Acknowledgement hand, patients with mild disease may also become frail due to a sedentary lifestyle during the isolation period. The authors would like to thank Dr. Kai-Hua Chen, the The rehabilitation protocols suggested in this expert Secretary-General of Taiwan Academy of Cardiovascular consensus, which are summarized in Fig. 1,improvespa- and Pulmonary Rehabilitation, for holding discussion tients’ quality of life after recoverydan aspect that meetings, recording the details of the meetings, and should never be overlooked during the management pa- miscellaneous tasks related to the publishing of this expert tients with COVID-19. consensus.

Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/ + MODEL Rehabilitation for COronaVIrus Disease 2019 9

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Please cite this article as: Cheng Y-Y et al., Rehabilitation programs for patients with COronaVIrus Disease 2019: consensus statements of Taiwan Academy of Cardiovascular and Pulmonary Rehabilitation, Journal of the Formosan Medical Association, https://doi.org/10.1016/ j.jfma.2020.08.015 http://guide.medlive.cn/